Traversa Parasites & Vectors 2012, 5:91 http://www.parasitesandvectors.com/content/5/1/91

REVIEW Open Access Pet roundworms and : A continuing need for global worming Donato Traversa

Abstract Ascarids and ancylostomatids are the most important parasites affecting dogs and cats worldwide, in terms of diffusion and risk for and human health. Different misconceptions have led the general public and pet owners to minimize the importance of these intestinal worms. A low grade of interest is also registered among veterinary professions, although there is a significant merit in keeping our guard up against these parasites. This article reviews current knowledge of ascarids and ancylostomatids, with a special focus on pathogenicity, epidemiology and control methods in veterinary and human medicine.

Review “common intestinal worms” and to erode the importance Background of the veterinarian in controlling parasites of veterinary The relationship between human beings and domesticated and human impact. This low-grade of interest and atten- small began about 15.000 years ago [1]. Such tion is crucial if one considers that several pet intestinal association has led to the dispersion of pets all over the are zoonotic and endemic globally, and the World, along with the spread of their pathogens. Some of spread of these parasites may be favoured by current them are common and zoonotic: as a consequence, there climate changes. In fact, these parasites have periods of is a continuing interest on their sanitary impact, and on development and survival in the environment, which are prevention and control methods. In the past few years the often at the basis of transmission routes in important attention of the Scientific Community has been attracted sapro-zoonoses. by feline and canine extra-intestinal parasitic nematodes, Different species of ascarids (commonly known as which are emerging in several countries and spreading “roundworms”) and ancylostomatids (commonly known into regions previously free from these parasites. Indeed, as “hookworms”) may affect the small intestine of dogs global climate change is influencing the ecology of and cats [7]. Actually, they remain the most important helminths with multiple hosts and different transmission parasites affecting companion animals worldwide and routes. As key examples, this is the case of the insect- maintain the primacy in terms of dispersion and risk borne filariae and eyeworm [2-4] and of the snail-borne for animal and human health. This is of particular lungworms Aelurostrongylus abstrusus and Angiostrongy- importance also because some driving forces are now- lus vasorum [3,5]. This new concern has caused the adays favouring their spread, e.g. the increase of wild misconception that intestinal worms of cats and dogs do fox populations in sub-urban and urban areas. For not deserve a high-standard level of attention anymore, example, wild foxes may act as reservoirs and amplifiers especially because the routine use of certain of canine ascarids, thus they re-enforce environmental is believed to have reduced their diffusion and impact on contamination and risk of infection [8]. animal health and welfare [6]. Indeed, the use of broad There is, in turn, a significant merit in keeping our guard spectrum drugs, which are sold (often over-the-counter) up against these nematodes even when other parasites are in a plethora of formulations, carries the risk that leads attracting attention and interest. Therefore, the aim of this the general public to minimize the importance of the article is to review the most important features of roundworms and hookworms affecting companion animals, along with critical and focused appraisals on the import- Correspondence: [email protected] ance of their pathogenicity, epidemiology and control Department of Comparative Biomedical Sciences, University of Teramo, Teramo, Italy methods in veterinary and human medicine.

© 2012 Traversa; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Traversa Parasites & Vectors 2012, 5:91 Page 2 of 19 http://www.parasitesandvectors.com/content/5/1/91

Intestinal nematodes are complex and interesting from the environment or tissutal larvae in paratenic Pets can be parasitized by different nematodes, intestinal hosts, e.g. rodents [13]. roundworms, hookworms and whipworms being the Pathogenesis and symptoms due to adult stages are most common. Main aspects of trichuroid whipworms similar to Toxocara spp. (see below) but the infection (i.e. Trichuris vulpis) affecting the large bowel of dogs does not occur in animals aged less than about 2 months. have been recently described elsewhere [9], thus this Prepatency period is about 10–11 weeks [20,21]. species will be excluded from this article. Among the most common hookworms, and Toxocara cati are the two major caninum and Ancylostoma tubaeforme are species-specific ascarids globally infecting dogs and cats, respectively. for dogs and cats respectively, while Ancylostoma bra- Both species have a complex and fascinating biological ziliense, Ancylostoma ceylanicum and Uncinaria stenoce- cycle, which relies on different pathways of larval phala affect both species [7,17,22]. In general A. caninum, migrations and transmission, depending upon mainly A. tubaeforme and U. stenocephala are spread especially in the source of infection and animal age. warm countries (Ancylostoma spp.) and in colder areas of Bitches are a major source of infection for their off- temperateandsubarcticregions(U. stenocephala)inboth spring because, after an infection occurs in their life, hemispheres; the remaining hookworms are most often they harbour somatic larvae. These resting larvae will present in sub-tropical and tropical countries [20,23-26]. As mobilize during pregnancies and infect subsequent for roundworms, hookworms have a complex biological litters even when re-infections do not occur. Pups cycle, in which different sources and ways of infec- become infected in utero by the second month of tion are possible. The most important infectious stage is gestation, which result in egg shedding after a minimum represented by filariform larvae present in the soil, which period of about two weeks after birth [10,11]. When infect a suitable host by actively penetrating the skin mobilized larvae are transmitted via the lactogenic route (especially for Ancylostoma spp.) and/or via the oral route litters can also be infected by colostrum and milk for at (i.e. Ancylostoma spp., Uncinaria spp.) [7,13,22,27]. least 38 days after delivery [12,13]. These vertical infec- Nursing is a relevant source of infectious larvae of A. tions occur regardless of the presence of the intestinal caninum for puppies. In fact, it is well established that, parasitosis in the bitch but, in general, a proportion of when infection occurs in adult dogs, a proportion of mobilized larvae may reach the intestine of the dam, larvae invade different body regions. These resting stages then mature and cause a patent infection with high egg survive for years and are, in turn, reactivated during shedding lasting weeks after whelping. Bitches can be re- oestrus and in the last 2–3 weeks of pregnancy, when infected also by ingesting immature ascarids defecated they are passed via the milk to the litter for at least by their suckling offspring. Therefore, lactation may either 3 weeks after delivery [26,28-30]. A bitch harbouring cause or reinforce a patent infection in bitches, which pro- somatic larvae is infectious for three consecutive litters, vides another source of environmental contamination and although the larval output is reduced in each lactation infection for puppies [13]. [30-34]. Conversely, there is a scattered and conflicting While T. cati is not transplacentally transmitted, lacto- body of bibliographic information on the transplacentary genic infection may occur in kittens during the first days of transmission [13,20,26,35,36]. Indeed, if in utero infec- nursing [14,15]. It has been recently shown that the acute tion occurs at all, it is obfuscated by the lactogenic route infection of the queen during a late phase of pregnancy and, in any case, prenatal transmission by A. caninum causes the milk-borne infection in the offspring [15]. does not occur in all puppies from a litter [7,27,37-39]. Dogs and cats of all ages can also acquire the infection It has also been reported that larvae of A. caninum dor- by ingesting Toxocara embryonated eggs from the envir- mant in musculature may be re-activated following fac- onment and eating paratenic hosts (e.g. invertebrates, tors driving stress, e.g. severe illness or corticosteroid ruminants, rodents, birds) harboring tissutal larvae therapies, which then reach the intestine causing patent [13,16-18]. infections in the adult dog [27]. In utero and lactogenic The prepatent period for toxocarosis by T. canis is at infections do not occur for A. tubaeforme, even though minimum 4–5 weeks after ingestion of embryonated eggs literature is scarce and the extent of milk transmission is or resting larvae, and 2–3 weeks for prenatal infections, stated to be not well known [7,17,27]. For the other while kittens start to shed T. cati eggs after about 7–8 weeks canine and feline hookworms vertical infections do not post infection [13,19,20]. appear to occur at all [7,17,39,40]. A third roundworm, Toxascaris leonina, affects both Paratenic hosts are also important in transmitting dogs and cats. This species is, in general, less diffuse ancylostomosis in dogs and cats which prey on ani- than Toxocara spp., especially because transmissions via mals (e.g. rodents). Prepatent period for A. caninum, the placenta and mammary glands do not occur. A. tubaeforme and U. stenocephala is about 2–3 weeks Animals become infected only by ingesting larvated eggs [7,17,20]. Traversa Parasites & Vectors 2012, 5:91 Page 3 of 19 http://www.parasitesandvectors.com/content/5/1/91

In summary, there are major factors making round- can be higher in dogs of more than 3 years of age than worms and hookworms the most common endoparasites in puppies of less than 4 months [60]. Surveys performed in pets all over the World. First of all, the possibility of in the USA have underscored high infection rates in puppies and kittens being infected by their dam by young puppies and only slight age-related decrease of transmammary and/or transplacental route/s is a power- prevalence after 1–2 [47] or 7 years of age [54]. It is worth ful host-finding strategy. Also, pups have daily thousands mentioning that, after resting larvae of A. caninum are re- epg counts for T. canis and animals often shed millions activated in pregnancy, they can cause auto-infection of of eggs for weeks, thus causing a high envir- the dam, thus reinforcing opportunities for adult dogs to onmental contamination. Ascarid eggs can survive for show patent ancylostomosis [13]. In general, old dogs years in extreme environmental conditions, thus are infected by A. caninum usually display a prolonged prepa- available for ingestion at any time. Infected paratenic tency and a reduced period of egg shedding, likely hosts are ubiquitous, being a constant source of infec- due to partial immunity or age resistance [13]. Given tion especially for cats, given their hunting instinct. that A. tubaeforme is not transmitted in utero or via the milk, the infection can be present in cats of all ages and not Is age a decisive circumstance for host-finding strategies only in kittens. There are studies that have shown an in- of intestinal nematodes? creasing trend of infection rate in 1–5 year old cats rather There is a long-standing misconception on the age cat- than in younger animals [42,53]. egories of dogs and cats, which can be infected. In fact, An investigation carried out in the USA on the most it is often thought that “intestinal worms” are only a common canine and feline endoparasites in thousands health problem of puppies and kittens and that adult of pets has shown that, after animals under 6 months of animals are, instead, resistant. age (as expected), the most parasitized category of The real truth is that pets are exposed to roundworm animals are patients more than 10 years old [53]. The and hookworm infections throughout the year and for possible explanation of such a high degree of all their life. Specifically, parasitic burdens, egg output in old animals may reside in a loss of immune response and infection rates are higher in puppies and kittens but against previously experienced parasites [61,62]. Another it is nowadays established that patent intestinal infec- possible reason may be a loss of compliance of pet tions occur in dogs and cats of all ages [41-50]. owners, who, perhaps, become less willing to engage in Adult dogs can be re-infected by T. canis even when chemopreventative measures in old pets [53]. Such under regular control programs [46,51]. Also, they have changing approach of pet owners should be discouraged the same susceptibility for patent infections as naïve by veterinarians not only for the pathogenicity of patients when later re-exposed and even when repeat- intestinal worms, but also because there is no practical edly exposed to the parasite and having circulating anti- reason to consider an old animal a less effective source bodies vs ascarid surface antigens [52,53]. Patent ascaridosis of infection for other pets and human beings in may be detected in animals older than 3 years or more, and comparison to puppies and kittens. may also establish when infection occurs with a few larvated ova [11,46,54-56]. Also, nursing bitches may Biology and pathogenicity of intestinal nematodes: present heavy patent infections by about 4 weeks after de- Threats for pets and humans livery [27]. Virtually 100% of dogs and cats, from the cosseted and Analogously, the chance that a cat develops a patent beloved pet to the stray animal, have been in contact intestinal infection by T. cati remains high throughout its with ascarids and ancylostomatids or, at least, are at risk life. For instance, one of the major causes of infection for of disease. adult cats is the ingestion of larvated eggs acquired from Ascarids live free in the lumen of the small intestine feed- the environment by their perpetual self-grooming [27]. ing on its content. Mild infections are usually not accom- For its biological cycle, the infection by T. leonina is panied by clinical signs either in larval migration or in much more common in adult animals than in young patent infections. When the number of canine roundworms subjects [27]. is moderate-high, larval migrations can cause cough, frothy Some studies have unwaveringly indicated a signifi- nasal discharge, pneumonia and edema of the lungs. Death cantly higher prevalence of canine hookworms in young mostly occurs in this larval phase and especially within a dogs [41,44,47,57]. Nonetheless, there is evidence that few days after birth in puppies borne after a severe prevalence of A. caninum in dogs <11 months of age transplacental infection [13]. Adult roundworms in pups can be significantly lower than infection rates in dogs cause by the second-third week of age a mucoid enteritis aged 1–6 and >6 years [58] and that there is no relation- characterized by vomiting, diarrhoea, ascites, anorexia, ship between host age and prevalence of Ancylostoma anaemia, unthriftiness, emaciation, poor coat, nasal dis- spp. [59]. Analogously, prevalence of U. stenocephala charge, and pot belly (Figure 1) due to heavy worm burden, Traversa Parasites & Vectors 2012, 5:91 Page 4 of 19 http://www.parasitesandvectors.com/content/5/1/91

worms are large and usually alive. Nursling puppies suffer severe discomfort, whimper and shriek and, when walking or standing, present a straddle-legged posture of the hind limbs [27]. Penetration of the peritoneal cavity after gut wall perforation, with subsequent peritonitis and massive blood loss, have also been reported [63,64]. Infected kittens may show a catarrhal enteritis with vari- able appetite, vomiting after feeding, diarrhoea alternated with constipation, developmental disturbances, anaemia and anorexia, especially after severe infections [65,66]. In adult cats T. cati may cause vomiting, enlargement of the abdomen, anorexia and even gastric perforation with presence of adult parasites in the abdominal cavity [67,68]. A case of a feline infection by T. canis characterized by an eosinophilic granulomatous dissemination of larvae has been reported in a pyrexic cat [69]. Toxascaris leonina has a less dramatic pathogenicity, but in dogs it may cause pica, digestive disturbances and reduced growth, while in cats the infection can be seen as an enteritis with vomiting and diarrhoea, even bloody [17,70,71]. Hookworms have been regarded as the most faithful intestinal parasites of dogs and cats [36]. Indeed, they are responsible for developmental impairment, severe clinical signs and high death rate, especially in young subjects. These worms live anchored to the gut mucosa Figure 1 Pot belly in a roundworm-infected puppy. by their oral capsule and have a relevant blood-sucking activity. Indeed, while A. braziliense may present a mild dysbacteriosis and gas formation. In severe circumstances pathogenic impact, the other hookworms are intensive animals may suffer from thickened intestine, partial or total hematophagous and cause important exsanguination. In obstruction or occlusion, duodenum dilatation, peritonitis, general, ancylostomosis in pets induces a mild enteritis bile and pancreatic ducts blockage, rupture of the intestine to a fatal hemorrhagic diarrhoea with , depending and worms at different stages expelled with the vomitus or upon different drivers, e.g. age of the animal, parasitic the faeces (Figure 2); indeed, pups and kittens with heavy burden and species involved [16,17,20,27,29]. infections may expel a large mass of worms in vomitus Juveniles of A. caninum burrow deeply and massively into [13,16,20,27], thus causing distress for the owner as the the mucosa, thus symptoms can be severe and life- threatening especially for puppies, in which even fatal diseases may occur in pre-patency. After a milk-borne infection, pups, which have low iron reserves, are healthy in the first week of age, and then show profound blood loss and deteriorate rapidly within the second-third week after birth. Age is a crucial factor in the outcome of canine ancylostomosis, because as the animal grows, resistance increases, regardless of whether the animal has experienced one or more infections. However, further infections may be inhibited by a pre-existent hookworm populations (i.e. premunition) and, in general, symptoms in adult dogs are dependent upon state of nutrition, hematopoietic capacity, presence of stressful conditions. In general, adults with a mild parasitic burden with A. caninum suffer with a moderate anaemia for the capacity to which their bone marrow has to compensate, Toxocara canis Figure 2 Adults of spontaneously expelled with but these animals may develop a more intense microcytic the faeces by a puppy. hypochromic anaemia in any case. Heavy infections always Traversa Parasites & Vectors 2012, 5:91 Page 5 of 19 http://www.parasitesandvectors.com/content/5/1/91

present with chronic iron deficiency anaemia, poor coat, may penetrate human skin, causing local lesions, intestinal loss of weight, bloody and mucous faeces, reduced growth, distress and even ocular/neurological signs; however, the circulatory collapse, lack of stamina and poor general aetiological role of each animal hookworm in causing dis- physical condition [13,20,27,36]. ease in humans remains to be elucidated (see next section). Cats affected by A. tubaeforme suffer with enteritis, blood loss, diarrhoeic faeces, reduced weight, regenerative anemia, Pet roundworms and hookworms are zoonotic cachexia and even death [13,65,72]. Soil-transmitted helminthoses affects more than 2 billion Uncinaria stenocephala has a less intense haematopha- people worldwide [85]. The zoonotic ability of Toxocara gous activity compared to Ancylostoma spp. and removes spp. has been established since the 1950’s [86,87] and small amounts of blood; heavy infections in young animals presently it is well known that pet ascarids cause human may be characterized by mild anaemia, hypoalbuminemia, infections globally, as demonstrated by several surveys anorexia, diarrhoea and lethargy [20,27]. carried out in all corners of the World [18,88]. The majority of canine and feline roundworms and Indeed, T. canis is largely acknowledged as a major hookworms are potentially zoonotic. culprit of human syndromes by animal ascarids, but it is Human beings can be hosts of ascarids when they inad- likely that some human infections are caused by T. cati vertently ingest embryonated eggs from the soil (i.e. sapro- as well [88,89]. zoonosis) or tissutal larvae. For instance, this happens by Some infections are asymptomatic [90,91] and the putting unwashed fingers into the mouth, or eating raw degree of damage and elicited signs depend upon the contaminated vegetables or meat of paratenic hosts [73]. tissue/s invaded, number of migrating larvae, host age and As an example, a relatively common source of human immune response. When symptoms are present, two infection is food, represented by vegetables harvested from major syndromes may occur, i.e. the so-called “visceral farms using animal dung as fertilizer [18,73,74] or by raw larva migrans” (VLM), encompassing important organs or undercooked liver or meat from ruminants, pigs, (mainly liver, lungs, brain) and “ocular larva migrans” chickens [18,75,76]. A relatively unexploited source of (OLM), due to damage to eye and optic nerve; other infection for humans is represented by embryonated ascarid minor syndromes, e.g. covert, neural, and atopyc eggs present on dogs’ fur [56,77]. The real proportion of toxocarosis, are also reported [88,90,91]. petswhosefuristrulycontaminatedbyinfectiouseggsand Children, in particular toddlers, are the most frequent whether they are a real threat for humans still remains to subjects suffering from VLM, often with severe clinical be elucidated. However, direct contact with an animal symptoms. The high occurrence in children is due to infected by roundworms should not be considered frequent exposure to areas (e.g. sandpits, sandboxes, hazardous for the following reasons: Toxocara eggs need gardens, playgrounds) potentially contaminated by Toxo- about 2–6 weeks before infectivity is reached, they are cara eggs and to low hygiene standards [79]. Also, geo- strongly adhesive on animal’s coats and difficult to ingest, phagic pica (e.g. due to iron or zinc deficiency or to most of them are not viable, and, finally, several fur grams behavior disorders), which may affect up to 10% of need to be swallowed to cause infection [78-84]. Moreover, children, is another relevant risk factor [79,92]. thepresenceofnon-canidparasiticovaonfurofdogs VLM in 1–5 year old children is characterized by fever, indicates that animals become contaminated in the leucocytosis, eosinophilia, hypergammaglobulinaemia, environment, possibly through scent-rolling, rather than general malaise, abdominal distress and pain; when from their own defecations [56]. larvae infect the liver, patients can suffer from hepato- Once infective elements are ingested, larvae penetrate megaly, granulomatous hepatitis or even necrosis [79,93- the gut wall and reach the bloodstream wandering 95]. There are cases of bronchiolitis/pneumonitis with throughout the body, i.e. eyes, heart, muscles, brain, wheezing, cough and asthma-like bronchospasm, and of lungs, liver. Thereby, larvae do not molt nor reach the myocarditis, nephritis, and involvement of the central adulthood but, however, induce severe local reactions nervous system with meningoencephalitis, seizures, and and damage, which may lead to different syndromes (see neuropsychiatric signs [79,88,94,96-98]. next section). OLM usually occurs without signs of VLM in children With regard to hookworms, pets and humans suffer from aged 5–10 years and in adults as well [92,99], and is a skin condition when free-living infective larvae species characterized by impaired vision to total loss of sight, due present in the soil, enter into the skin to reach the intestine to endophthalmitis, retinal granulomas and detach- via the bloodstream. In pets the cutaneous damage leads to ment of the macula [88,100]. Other signs are complaints of different degrees of itching, erythema, vesicular or papular “seeing lights”, squint and glaucoma; more importantly, lesions, acanthosis, hyperkeratinization, cellular infiltrates OLM may mimic a retinoblastoma, thus erroneously indu- and perivascular cuffing, especially at the interdigital skin cing enucleatio bulbi [99,101,102]. Hundreds of cases of [22,26,36]. However, infectious larvae of animal hookworms unilateral blindness and of more or less severe eye damage Traversa Parasites & Vectors 2012, 5:91 Page 6 of 19 http://www.parasitesandvectors.com/content/5/1/91

have been calculated to occur yearly in US childhood due Indeed, A. tubaeforme does not penetrate human skin to OLM and dozens of unnecessary eye enucleations due to or has a little skin penetration and, although A. caninum misdiagnosis with retinoblastoma are described [6,27,74]. and U. stenocephala are indicated as cause of CLM, their A third condition, called “covert toxocarosis”, might role as agents of skin lesions in humans is still unclear be caused to long-term exposure to migrating larvae in [26,36,116,118,119]. There is an old report of a self- specific target organs. In children older than toddlers, infection by larvae of U. stenocephala, which showed this form presents vaguely with behavioral changes, that they can penetrate human skin [120]. Skin penetra- seizures and sleep alterations, cough, asthma, abdominal tion by larvae of A. caninum has been associated with discomfort, headache, while in adults it may present follicolitis, ephemeral and papular/pustolar eruptions with weakness, rash and itching, abdominal pain and [121-123] and to the penetration of muscle fibers and breathing distress [103-108]. lung infiltrates [124]. However, this latter identification Finally, skin conditions, like pruritus, urticaria and dif- was grasped on epidemiological and biological bases and ferent eczematous lesions, have been found in association not on a specific identification of the parasite [124]. In- with toxocarosis in both childhood and adults [88,109]. deed, myositis occurred in human volunteers after skin There are reports of juveniles of feline roundworms infection by larvae of this canine hookworm [125], thus identified in the liver and the brain of two children from corroborating the hypothesis that larval A. caninum may the USA and Israel [110,111]. Interestingly, there are indeed cause muscular damage. These larvae have also published cases of adult T. cati passed from the anus or been associated with a sort of human OLM, a unilateral the mouth of children, but it is very likely that these sub-acute neuroretinitis with loss of vision [126] and, as cases originated by an altered behavior, i.e. taking worms those of A. ceylanicum, can reach adulthood in the from vomitus or faeces from an infected animal human gut. In particular, a relatively newly discovered [112,113]. It seems that T. leonina does not display human disease caused by A. caninum is an eosinophilic zoonotic potential. However, there are a couple of enteritis regarded as an emergent disease in some areas, published reports of possible human infections by this e.g. Australia and USA. This syndrome, not known species: a case of osteomyositis with cutaneous abscesses before the 1990’s [126-128], poses important diagnostic containing worms identified as T. leonina has been challenges. It can be even caused by a single hookworm described in the 1960’s in the former USSR [114], while in the intestinal lumen and is characterized by a case of ocular infection by a suspected Toxascaris spp. abdominal pain, discomfort and distension, weight loss, larva has been described from Africa [115]. diarrhoea and rectal bleeding [22,128-130]. Occasionally Humans may be infected by free-living hookworm larvae also A. ceylanicum can develop to adult stages in human when walking barefoot, when in close contact with poten- bowel, causing intestinal distress [22,131]. tial contaminated soil (e.g. gardeners), or when sunbathing on beaches in risky areas. Larvae of A. braziliense cause the Treatment and control methods: Need for compromises? so-called “” (CLM), a dermatitis Different parasiticide classes are available for treatment with long serpiginous and persistent tracks underneath the and control of intestinal nematodes, being (pro-) benzimi- human skin. The role of other hookworms in causing CLM dazoles (e.g. febantel, ), tetrahydropirimidines needs to be clarified. The US CDC states “CLM” to be (e.g. pyrantel), cyclooctadepsipeptides (i.e. emodepside) known also as “creeping eruption”,being“a zoonotic infec- and macrocyclic lactones (e.g. ivermectin, , tion with hookworm species that do not use humans as a moxidectin, milbemycin oxime) the most used. definitive host, the most common being A. braziliense and Provided below are some key examples of major mole- A. caninum” [116]. Also, the CDC states that “Alarger cules available for treatment and control of ascarids and group of hookworms infecting animals can invade and ancylostomatids. parasitize humans (A. ceylanicum) or can penetrate the A comparative study evaluated the efficacy of three for- human skin (causing cutaneous larva migrans), but do not mulations containing mebendazole or fenbendazole alone, develop any further (A. braziliense, A. caninum, Uncinaria or febantel in association with pyrantel and with the stenocephala)” [116]. cestocide praziquantel [132]. All formulations proved to be Indeed, the geographic distribution of CLM overlaps effective against infections by ascarids and ancylostomatids that of A. braziliense [25,117] and interestingly, it does not in dogs, with different therapeutic efficacies, up to 100% occur where this species is absent, e.g. in Mexico, West [132]. A multi-centric investigation indicated that the US coasts and Australia [24,26]. These epidemiological combination of febantel, pyrantel and praziquantel has an features have led us to consider A. braziliense as the only efficacy of ~99.9% against canine T. canis and hookworms species causing human CLM, although CLM-like cases [133]. Another recent study has demonstrated the efficacy have been reported from India, a country where A. brazi- and safety of tablets containing pyrantel, oxantel, and liense is not present [26]. praziquantel against natural and/or experimental infections Traversa Parasites & Vectors 2012, 5:91 Page 7 of 19 http://www.parasitesandvectors.com/content/5/1/91

by T. canis, A. caninum and other canine endoparasites against adult T. canis and T. leonina and in reducing [134]. In cats an association containing pyrantel and the fecal excretion of T. canis eggs in dogs as well praziquantel has high efficacy against ascarids and ancylos- [150]. A series of field investigations carried out in tomatids [133,135]. the USA and Europe demonstrated the safety and ef- Recent experimental and field studies have evaluated ficacy of the monthly topical administration of the the cyclooctadepsipeptid emodepside. Emodepside is same ML in the treatment of experimentally and available in a spot on formulation for cats (containing also naturally acquired ascaridosis and ancylostomosis in praziquantel), which has efficacy up to 100% in treating cats [151,152]. infection by T. cati or T. leonina at different stages A spot-on formulation containing the endectocide [136,137]. This formulation also has 100% efficacy against moxidectin together with the ectoparasiticide imidaclo- mature A. tubaeforme and efficacy of >95% and >97% prid has high efficacy against canine intestinal nema- against L4 and immature adults, respectively [138]. Tablets todes in mono-specific and mixed infections [153,154]. marketed for dogs containing emodepside (and prazi- For example, in the aforementioned multi-centric study quantel) have been shown to be safe and efficacious [133] this spot on formulation showed 98.8% efficacy >92-99% against natural or experimental infections against T. canis and 99.9% against . caused by L3s and/or L4, immature and mature adults of The same spot on formulation has 100% efficacy against canine T. canis and T. leonina [139]. Four different labora- adult stages of T. cati, up to 98.3% efficacy against im- tory investigations have demonstrated that this association mature adults and fourth-stage larvae of the same as- has >95% and >98% efficacy against larval and adult carid, and up to 100% efficacy against adult stages of U. stenocephala and A. caninum, respectively [140]. A mul- Ancylostoma and immature adults and third-stage larvae ticentre study evaluating the same association of A. tubaeforme [133,155]. showed high efficacy in reducing egg counts (i.e. geometric The ML milbemycin oxime also has high efficacy in mean egg counts reduced by 99.9-100%) in dogs infected removal of roundworms and hookworms from naturally by T. canis, T. leonina, U. stenocephala, A. caninum,under infected dogs and cats with patent infections [156,157]. field conditions [141]. Emodepside is also present in a For instance, adults of A. caninum and T. canis in natur- newly marketed oral suspension for dogs, also containing ally infected dogs are killed by milbemycin oxime the triazinetrione derivative toltrazuril for the simultaneous [158,159]. The molecule has been shown to be effective treatment of coccidiosis. This formulation has shown effi- also in experimental ascaridosis of pups [160] and to cacy of ≥94.7-99.3% and 100% against immature and adult have a certain degree of activity against canine ancylos- stages of T. canis respectively, and of ≥99.5-100% against tomosis [161,162]. In other trials the molecule has been adults of A. caninum and U. stenocephala, respectively, ori- proven to be active against T. cati [163] and fourth-stage ginated from natural and experimental infections [142]. A larvae and adults of A. tubaeforme in cats [164]. Milbe- multicentre investigation carried out across Europe has also mycin oxime is available in associations either with lufe- indicated efficacy of 100% and 99.9% against T. canis and nuron or praziquantel. In dogs, the oral associations of Ancylostomatidae based on faecal egg count reduction milbemycin oxime with lufenuron has shown 91.5% effi- [143]. This oral suspension for dogs has been also proved cacy against naturally ascaridosis [165]. In the multicentre to be effective in experimental feline infections by T. cati field study mentioned earlier the association containing and A. tubaeforme [144]. milbemycin oxime and praziquantel has achieved geomet- With regard to macrolactones, the efficacy of a chew- ric mean egg counts reduced by 99.4%-99.8% in dogs able formulation containing ivermectin (and pyrantel) infected by roundworms and A. caninum [141]. In against natural or induced roundworms and hookworms cats, this association has efficacy up to 96.5-100% in dogs has been documented to range from 90.1% to against fourth-stage larvae and adult stages of T. cati 99.6% [145,146]. This association is effective also in the and of 93.5% against hookworms [135,166]. treatment of dogs experimentally infected with A. brazi- Furthermore, milbemycin oxime has been recently liense [147]. In cats with mixed infections, an ivermectin- marketed in a monthly, chewable, tablet for dogs, also based chewable formulation showed 92.8% and 90.7% effi- containing the insecticide spinosad. This formulation cacy, respectively, against adult stages of A. braziliense has a 99.3-100% efficacy in treating and controlling in- and A. tubaeforme, while the number of eggs per gram of testinal nematodes in naturally and experimentally feces decreased 98.1% by 7 days after administration infected dogs [167,168]. [148]. What emerges is that veterinarians have a broad By 2000’s the endectocide selamectin has demon- spectrum of parasiticidal formulations that can be strated efficacy and safety against these parasites [149]. selected according to each individual possible scenario For instance, studies in experimental and natural infec- and owner and animal compliances. For instance, good tions have demonstrated the efficacy of topical selamectin compliance (i.e. 87.5%) of the owned pets treated with Traversa Parasites & Vectors 2012, 5:91 Page 8 of 19 http://www.parasitesandvectors.com/content/5/1/91

oral tablets containing pyrantel/oxantel/praziquantel has Puppies should wormed with safe formulations able to been documented [134] and, analogously, practices across kill the parasites and to reduce egg shedding in the Europe have reported a high acceptance by dogs trea- environment. As an example, a recent study has shown ted with the oral tablets containing emodepside [141]. the efficacy of two associations, i.e. milbemycin oxime- The oral suspension containing emodepside and tol- based (99.9%) and febantel/pyrantel -based (98.5%), in trazuril has an acceptance rated as good and medium reducing shedding of Toxocara eggs [173]. Given that in 90% and 9% respectively, in dogs treated in the multi- the lactogenic transmission lasts at least 5 weeks post center study mentioned above [143] and high palatability partum, treating puppies at two, four, six and eight when administered in cats [144]. Flavoured chewable weeks of age, and then monthly until 6 months of age tablets containing milbemycin oxime presented also high may suppress shedding of T. canis eggs in the whole acceptance by treated animals, going from 64% to 94.8% period of puppy-hood. The need for a frequent parasiti- directly from the owners’ hand [141,169]. Hence, sev- cide administration in pups is due to the continued eral oral formulations, due to their tasty flavor, allow exposition to re-infections, via the milk and the environ- a treatment with minimal distress to the animal and ment, and to the fact that they may already harbor the owner. migrating larvae after birth. If a parasiticide is not admi- It is worth noting that the formulation containing moxi- nistered within the 4th week of age, female ascarids may dectin and imidacloprid has the advantage of the easy-to- reach the adulthood and become gravid, thus eggs are apply dermal spot-on administration in parasitized dogs shed by the pup when it is as young as about 21 days. [170]. This is important also in feline clinical practice, given No transplacental transmission occurs in cats, thus that indocile or feral cats refusing oral formulations can be kittens can be subjected to fortnightly treatments by the easily treated with the spot-on containing moxidectin or 3rd week of age. Given that re-infections may occur emodepside [171,172]. throughout the suckling period, dams should be treated The use of antiparasitic molecules should be pro- with their offspring for the first 2–3 months to avoid grammed also according to other factors, related to the patent infections in nursing animals [13,16,17,27]. biology and their epidemiological features in Treatment of pregnant and/or lactating animals is different regions. Geographical spread of these parasites, facilitated by the availability on the market of molecules their clinical importance, and especially the high resistance which can be administered safely in different time peri- of infectious stages in the environment regardless season or ods or for the whole pregnancy and/or lactation, for climate (e.g. ascarid ova resist to harsh chemicals, broad instance pyrantel or milbemycin oxime, or other broad temperature ranges and several degrees of moisture), spectrum drugs. On the other hand, treating pregnant suggest careful attention to prevention approaches [13,88]. dams is questioned, although sometimes advised in some Puppies have been considered in the past as the main focus worm control programs [13,174,175]. Prolonged daily for antiparasitic treatments to control ascarids. However, administration of fenbendazole can reduce prenatal the demonstrations that intestinal nematodes may indeed infection but such regimen is expensive and can suffer infect adult pets and that animals which have been from lack of compliance by the owner [13,176]. Less- vertically infected by T. canis are more susceptible to re- frequent administration of ML, can be effective in inter- infections if compared to naïve dogs [13,18,46] change our rupting vertical transmission with different schemes of perspective in focused control programs. Also, adult cats treatment [13]. Despite the absence of label claims, such maybeoftenre-infectedbyT. leonina, especially if they go an approach could lead to increased compliance of the outside for hunting [17]. These cats are also more suscep- owners [13]. tible to infection by A. tubaeforme, because they can eat Owners and veterinarians should always thoroughly contaminated grass or larvae while grooming, or because follow manufacturer’s indications for each of the selected larvae can penetrate their skin when they are out- parasiticides administered to bitches, queens, puppies doors. Obviously, the same risk to of being infected and kittens. by A. caninum is run by adult dogs when living or Other than these general scientific concepts, indications walking in contaminated areas. from the US Companion Animal Parasite Council (CAPC) Regular “de-worming” or “worming”, an imprecise term and the European Scientific Counsel Companion Animal but common in daily language today [13], is the basis for Parasites (ESCCAP) should be taken into account. These an effective chemoprophylaxis irrespective the age of the two organisations have published guidelines for treatment pet. and control of major parasites affecting companion Taking control of ascarids as the key example, the animals [68,177]. major sources of infection and contamination are pup- Treatment of puppies and kittens at two, four, six and pies from 3 weeks and 6 months of age and nursing eight weeks of age is suggested by CAPC. Thereafter, bitches. animals should be put on monthly preventives as soon Traversa Parasites & Vectors 2012, 5:91 Page 9 of 19 http://www.parasitesandvectors.com/content/5/1/91

as label recommendations allow. Indeed, kittens do not infections in pet populations has been found after an- need to be treated for ascarids until 6 weeks of age but, nual or bi-annual anthelmintic treatments [51]. In this given the risk for , it is suggested latter study more than a half of a Swiss canine popula- they are treated at 2 weeks of age and then placed on tion has been found to shed helminth eggs at least once the monthly scheme using molecules effective in pre- in 1 year despite quarterly deworming. More specifically, venting heartworm infections and having efficacy against a yearly incidence of 32% of T. canis infection has been roundworms as well. If puppies and kittens are not trea- found in dogs that received four anthelmintic treatments ted until 6 to 8 weeks of age or later, they should be put per year [51]. on a monthly preventive according to label recommen- As mentioned earlier, in US settings the routine dations, dewormed again in 2 weeks, and then maintained monthly parasiticide administration is sometimes per- on monthly preventives thereafter [68]. In other words, a formed along with annual or semi-annual fecal examina- lifelong preventative program, using a “monthly-interval” tions [47,68]. (i.e. parasiticide administration at 4-week intervals, in ac- In any case, the monthly treatment approach appears cordance with the pharmacokinetics of the molecule used) to have several benefits, especially when performed with is supported to exclude any risk of infection for the own- a macrolactone, which can accomplish the suppression ers [13]. The veterinarian should monitor and evaluate the of most important parasitic nematodes affecting pets efficacy of i) initial treatments, ii) monthly control [179]. product, and iii) client compliance by 2–4 fecal examina- On the other hand, the possibility of using a year tions in the first year and 1–2 examinations per year round treatment is particularly important in those thereafter [68]. regions where there is a systematic necessity to perform The ESCCAP recently advised that pups should re- the annual chemoprophylaxis for other major parasites. ceive a parasiticide at 2 weeks of age, then at fortnightly A year-round control program with molecules which intervals until two weeks after weaning. Thereafter, pup- can be monthly administered for the prevention of pies should undergo monthly treatments until six cardio-pulmonary nematodes, i.e. Dirofilaria immitis months old. Fortnightly treatment of kittens can start at (e.g. ivermectin, moxidectin, milbemycin oxime) and 3 weeks of age and should be repeated fortnightly until Angiostrongylus vasorum (i.e. moxidectin), is powerful two weeks after weaning, then monthly for six months. also to achieve a decrease in prevalence of intestinal With regard to adult dogs and cats, annual or twice nematodes [49,180]. yearly treatments for Toxocara spp. does not reduce the A year round program would be powerful also in feline risk of patent infections and, also, worming four times a patients, given that the level of nematode transmission is year does not necessarily eliminate patent infections; higher in free-roaming cats than in cats which receive conversely, the ESCCAP states that monthly worm treat- adequate sanitary care [181]. However, recent studies ment can largely prevent patent infections [177]. In have proved high prevalence rates, at least for T. cati, other words, a treatment frequency of at least 4 times also in pet household cats [182-184]. per year, or at intervals not exceeding 3 months, or even The other side of the coin says that frequent use of a monthly treatment, are general recommendations, anthelmintics in companion animals could have according to different scenarios, e.g. real zoonotic risks, detrimental effects. In the past decades the abuse of presence of children in the pet owners family, pregnancy parasiticides has led to the emergence of livestock and of bitch or queen, housing conditions [13,177]. When a horse parasites resistant to one or more anthelmintic year-round-control is not performed (e.g. because an classes. As a general approach, the administration of a owner disagrees with a frequent anthelmintic adminis- broad-spectrum parasiticide without a copromicroscopic tration, or local legislation requires diagnosis or risk as- examination should be discouraged considering that the sessment prior to treat an animal), regular faecal unnecessary use of anthelmintics has major influence in examinations (e.g. every 1–3 months) of susceptible ani- promoting drug resistance. Hence, a concern related to mals is considered a feasible way of evaluating the re- frequent anthelmintic treatments could be an increase of occurrence of intestinal nematodes [177]. drug resistant populations of pet nematodes, especially A compromise between these two views from North for long-term indiscriminate use of parasiticides, which America and Europe seems to be a good choice [13], if have been on the market (often over-the-counter) over a particular situations do not apply. A minimum number long time. Indeed, at the moment there is only evidence of 4 administrations per year or treatments at intervals of resistance to pyrantel in A. caninum [185]. Although of 4–6 weeks can be effective in preventing most patent pyrantel is not used for monthly prevention of cardio- infections, while a worming frequency of less than 3–4 pulmonary parasites and no data have emerged for times per year does not influence parasite prevalence roundworms, a high level of attention should always be [13,178]. Nonetheless, no impact on patent parasitic maintained to detect any hint of drug resistance in pet Traversa Parasites & Vectors 2012, 5:91 Page 10 of 19 http://www.parasitesandvectors.com/content/5/1/91

nematodes. This is even more relevant considering that of gastrointestinal symptoms (e.g. diarrhoea, vomiting, there is the first laboratory evidence that D. immitis can etc.). This is of importance given that, for instance, no develop a degree, although yet to be established, of sur- significant differences in nematode infection in symp- vival to certain parasiticides [186]. tomatic dogs, compared with animals without clinical The present very limited evidence of drug resistance in signs has been found [49,53,192]. However, asymptom- small animal parasites is likely due to the fact that pets atic animals are usually considered parasite-free, thus are most often kept individually or in small numbers, their owners may be not interested in routine examin- thus dynamics of parasitic populations and influence on ation for parasites with subsequent treatment if neces- refugia is very different from what happens in livestock. sary [59]. Such an approach should be discouraged, Pets are usually treated individually, thus most round- given that asymptomatic dogs are as likely to be infected worms and hookworms in a given area escape from the as animals with clinical evidence. Therefore, these treatment and remain in the refugium [13]. Nonetheless, categories present the same level of zoonotic risk, which the indiscriminate use of anthelmintics in concentrated may not be fully appreciated by pet owners [59,193-195]. groups of small animals (e.g. kennels, colonies, shelters, There are, however, situations where awareness of pet breeding facilities) might nurture the development of re- owners on zoonotic diseases is very high and they accept sistant nematodes [187]. to have their pets undertaken on regular control plans [47,196]. Furthermore, repeated faecal examinations The importance of copromicroscopic examinations throughout the lifespan of a pet are of paramount The misconceptions that only young animals should be importance even in well- cared for dogs and cats, given dewormed and a single treatment clears a “generally” that recurrence of parasites is possible, regardless of parasitized animal, induce negligence in performing whether they undergo a control anthelmintic program diagnostic copromicroscopy in veterinary practices. or not [51,53]. Conversely, systematic copromicroscopic examinations From a practical standpoint, the pneumonic phase of should be regularly instituted for companion animals, larval migrations can only be suspected for the which, in turn, are virtually subjected for all their life- simultaneous appearance of respiratory symptoms in all span to continuous re-infection by roundworms and puppies of a litter within two weeks after birth. Specific hookworms, even when they have a lifestyle far from diagnosis of patent toxocarosis is achieved through stand- that of stray animals or of animals kept in shelter or ard copromicroscopic floatation because eggs of T. canis, refuges [47,188-190]. T. cati and T. leonina (Figure 3) are usually present in Copromicroscopic techniques, e.g. floatation methods high number and easy to identify. However, in certain or commercial kits, are easy to perform in clinical areas of the World (e.g. North America) the raccoon practices. Nonetheless, diagnostic challenges may arise roundworm procyonis can pose diagnostic for both ascaridosis and ancylostomosis. Pre-patency challenges. This ascarid causes patent infections also in period greatly affects diagnosis and effective control pro- dogs [197,198], and its eggs greatly resemble those of grams: parasitic ova can be detected at faecal examin- T. canis, thus representing a diagnostic problem and an ation only after nematode development, mating and important danger for human health. In fact, the vast patency, i.e. in some cases even a few weeks post infec- majority of humans who ingest infective eggs of B. procyo- tion and appearance of clinical signs. As a key example, nis suffer from severe permanent neurological damage or it has been shown that the vast majority of dogs aged even die [199]. Hence, at least where this parasite is less that 6 weeks are infected by intestinal roundworms, endemic, veterinary personnel must be skillful and trained although they may score negative at the copromicro- in recognizing eggs of B. procyonis for preservation of the scopic examination [6,191]. The same challenge may public health of people eventually exposed to faeces elimi- occur in puppies infected by hookworm larvae origi- nated by dogs infected by B. procyonis.Eventhoughthisis nated from their dam, in that these nematodes shed eggs true for North America, this parasite has been introduced by the tenth day of infection, thus after the symptoms also in Europe and Asia with its natural wild host [200]. appear. Diagnosis in these pups may be achieved only on Hence, what the future will hold on this life-threatening clinical signs like, for instance, pale mucosae and soft to zoonosis in other continents is currently unknown. liquid dark faeces. Also, symptoms caused by acute Diagnosis of ancylostomosis in dogs and cats cannot ancylostomosis due to sudden exposure to infective lar- be achieved at the species level for the overlapping vae in whelps and adults may appear about four days morphological and morphometric features of Ancylostoma before egg shedding, thus making diagnosis very prob- spp. eggs (Figure 3). Coprocultures can be performed for a lematic [16,27]. specific diagnosis but, from a practical standpoint, the Faecal examinations should not be related to patient’s presence of hookworm eggs in pets’ faeces would require health and must be performed regardless of the presence a parasiticide treatment regardless of the species affecting Traversa Parasites & Vectors 2012, 5:91 Page 11 of 19 http://www.parasitesandvectors.com/content/5/1/91

Figure 3 Floatation with zinc sulphate: eggs of Toxocara canis (A), Toxocara cati (B), Toxascaris leonina (C), Uncinaria stenocephala (D1) and Ancylostoma caninum (D2). the animal. Eggs of U. stenocephala (Figure 3) can be animals and to minimize public health hazards. All identified by their larger size [36]. categories involved in pet medicine should take care of Veterinarians should convince pet owners of the import- animal health and public behavior, given that human ance of periodic faecal examinations. In the first year of life syndromes caused by pet nematodes may lead to any pet should undergo at least 2–4 copromicroscopic permanent damage [18,88]. examinations and then, when adult, it should be examined Awareness of pet owners and the general public and more than once per year according to health status, lifestyle continuous education of veterinarians are at the basis of and frequency of treatments. Specifically, free ranging effective prevention. Dissemination of understanding animals and those living indoors but allowed to go and knowledge of transmission routes, at-risk categories outside should always be subjected to regular examination and areas, and control methods are pivotal to minimize of the faeces. Particular attention should be given to possibilities of human and animal infections. Although copromicroscopic analyses carried out in the worm con- virtually all of the majority of roundworms and hook- trol programs. When a monthly-based treatment program worms affecting dogs and cats may cause human is not performed, faecal examinations every 1–3months diseases, the public risk perception in general is poor. As of susceptible pets is an efficacious way of evaluating a key example, despite the infection by Toxocara spp. is the re-occurrence of intestinal parasitoses in previously the most prevalent human helminthosis in some indus- treated animals. Indeed, post-treatment faecal examina- trialized countries, public awareness of this syndrome is tions are important to evaluate success of drug admin- scant [201]. A survey carried out in the UK has shown istration and, in a future perspective, to detect any than less than the half of the people interviewed, includ- indication of drug resistance in ancylostomatids and ing pet-owners and non-pet-owners, perceived the risk ascarids. On the other hand, coprophagy is relatively of transmission of nematodes from pets to humans. commonindogs,thusthepresenceofeggsinstool Interestingly, no differences in hazard awareness was samples after treatment could often be due not to found between people who owned a pet and people who failure of treatments but rather to ingestion of their did not [202]. Another study performed in a developed own defecation or other animals’ faeces [84]. area of Brazil has demonstrated that the majority of dog owners did not know about intestinal parasites, sources Awareness of the general public and pet owners: A need of infections, possible risk factors for zoonoses and fo- to enhance risk perception without causing alarm cused prophylactic measures. Therefore, the high pres- Controlling ascaridosis and ancylostomosis in pets is ence of zoonotic species in owned dogs of the crucial to reduce infection risk for other companion studied region, along with the lack of information Traversa Parasites & Vectors 2012, 5:91 Page 12 of 19 http://www.parasitesandvectors.com/content/5/1/91

known by owners, endorse that the risk of zoonotic With regard to hookworms, sites favoring survival and infection by canine intestinal nematodes may be in- development of free-living larvae are shaded, warm, deed high [59]. humid and well-drained soils. Furthermore, unpaved Veterinarians, who are the most appropriate and ques- runs are highly favorable for hookworm larvae because tioned source of information on zoonoses, should always of mixing of faeces and soils. Prevention of animal and provide pet owners with accurate worming schedules human ancylostomosis relies on adequate hygiene and their efficacy, and appropriate all-day-life measures. measures (e.g. hand and feet washing), removal of pet This is of particular importance if one considers that faeces and, importantly, wearing shoes and avoiding veterinarians are a more congruous source of knowledge lying on risky areas or, in any case, where there is the on zoonoses than physicians [203]. Nonetheless, lack of likelihood that animals usually defecate. education has been well documented also in veterinary professions [203-205]. In Canada less than the half of Hookworms and travelling practitioners working in small animal practices declared Tourists travelling in at risk zones for CLM should be that they talked with pet-owners about the zoonotic risk careful in walking barefoot on beaches and in lying of pet endoparasites, while the remaining did so only down on the sand, especially because A. braziliense is under particular circumstances or did not at all [206]. In endemic in popular tourist areas. These human categor- the USA it has been recently suggested that a national ies are susceptible to infection at their vacation destin- surveillance program should be established in order to ation and then may return home infected at the end of better understand specific aetiology of human larva the holiday, often providing a challenging dilemma to migrans syndromes and their actual incidence, in order their physician. to aim for focused intervention programs [18]. More Nonetheless, autochthonous reports of CLM have been interview- based studies are warranted in other countries reported from countries where the tropical A. braziliense to implement our understanding of how the risk percep- is absent, thus these cases are considered “unexpected” tion is diffused in the population and, more importantly, [26]. Unfortunately no identification to species of larvae to implement awareness of the general public and of pet found at biopsies has been performed, thus only hypoth- owners. eses are available on the identity of hookworm involved. No practical methods exist to eliminate infective As key examples, CLM cases possibly by U. stenocephala elements of intestinal nematodes of pets (especially for and/or A. caninum have been recorded in the UK and ascarids) present on the ground, thus prevention of New Zealand. Several other local cases of CLM by initial contamination of the environments is the key unidentified hookworms have been described in Italy, goal. Veterinarians should inform all owners about ways Serbia, Germany, France and UK as well [26]. Although of transmission for their pet and for themselves, and few in number, these cases in areas where A. caninum, about clinical evidence for diseases and methods of A. tubaeforme and U. stenocephala are present, show a prevention. On the other hand, any pet owner should possible risk for human infections, characterized by clearly acquire relevant information and have appropri- skin conditions, which, possibly, could also involve ate behavior. In fact, an important cause of the heavy other conditions (e.g. pneumonitis). Also, it cannot be outdoor presence of infectious parasitic elements is lack ruled out that these few cases published could be the of education (and of awareness on the actual zoonotic tip of the iceberg and that others are not diagnosed or risk) by pet owners. Sites shared by children and animals not even referred to physicians. The number of CLM in like backyards, sandpits, parks, playgrounds, beaches, “unexpected” countries could be much higher than often represent a risk for the heavy contamination by thought, thus not only travelers and tourists spending pet faeces. Public parks may be highly contaminated by holidays in tropical zones considered “risky” can be eggs of T. canis, while sand-boxes and sand-pits by those faced with these infections but all humans exposed to of T. cati [18,88,90,207,208]. Hence, common prevention soil contaminated by larval hookworms. practices, which should be known by any pet owner are covering sandboxes, avoiding animal defecation in public Conclusion areas or at least always clean animal faeces from the Given the clinical importance of intestinal nematodes ground. In fact, educating owners on regular removal affecting pets, their ubiquitous presence and the and disposal of faeces and to empty cat litter trays is of zoonotic impact some of them have, public education is paramount importance to minimize environmental con- crucial for reducing risk exposure in both humans and tamination and risk of transmission to both animals and companion animals. At the same time pet owners and, humans [6,79]. When walking their pets in public areas, in general, the public opinion should maintain a self- all owners should respect local indications (Figure 4) confidence that keeping a pet is safe and a positive ex- and keep their animals in reserved areas, if present. perience. This is also true when close-contact occurs Traversa Parasites & Vectors 2012, 5:91 Page 13 of 19 http://www.parasitesandvectors.com/content/5/1/91

Figure 4 Dog-reserved areas and indications for pet owners in public areas in Valencia, Spain (A), Praha, Czech Republic (B) and Melbourne, Australia (C).

between the pet and the owner, even when some behav- present [212,214]. However, the potential risks of pet- iour can be questionable (Figure 5). Actually, it is estab- originating zoonoses should always be kept in mind. lished that direct contact with infected pets presents no This has become even more so in recent years, when relevant risk in the transmission of intestinal nematodes several sociological changes have influenced the relation- and there is no association between pet ownership and ships between physicians and veterinarians. In fact, the infection occurrence [78,79]. Owners should have confi- major goal of the re-discovered “One Health Program” dence that ownership of any companion animal is bene- (i.e. “the collaborative work of multiple disciplines to help ficial and safe as long as their pets are healthy [18]. Pet attain optimal health of people, animals, and our owners enjoy a plethora of advantages by living with environment”) highlights the crucial role of a tight tie dogs and/or cats. For instance, children, the elderly and between the human health operators, vet practitioners, disabled persons particularly benefit from their contact and the general public [213]. with a beloved pet. Companion animals represent a way For instance advances in chemotherapy for AIDS and of life for a lot of the people and this relationship new possibilities of organ transplants, and the provides socialization, mental health, and physical well- prolonged life expectancy, have increased the number being: those who own a pet have been shown to display of immunocompromised patients in human communi- reduction in blood pressure and cholesterol levels, ties. These subjects need to be aware of possible require less medical care, and it has also been reported zoonotic parasites and of all measures to prevent that there is an improvement of life quality and quick infections for their pets and for themselves. It is worth recovery after heartbreaking events [209-213]. Therefore, highlighting that immunocompromised individuals owning companion animals is vital for the majority of should not give up their animal, as it has been demon- families, especially when children and the elderly are strated that pet ownership minimizes depression and Traversa Parasites & Vectors 2012, 5:91 Page 14 of 19 http://www.parasitesandvectors.com/content/5/1/91

Figure 5 Close contact between privately owned pets and their owners. Although this behavior can be questionable, it cannot be considered at risk of infection with zoonotic nematodes for the owners.

that standard hygiene measures reduce at minimum the public and private grounds and litter trays, alimentary risk of acquiring zoonotic infections in this particular habits [216-218]. category [215,216]. Ten years ago it was perceived that veterinary parasit- A desirable goal for effective control programs would ology was becoming irrelevant in routine clinical practice also be to understand which are changes and trends in [219]. Regrettably, after more than ten years this perception terms of prevalence of infection by ascarids and hook- is practically a reality in several settings. The involvement worms in canine and feline populations, with the simul- of practitioners in a worming control program is no more taneous aim to track incidence of human cases caused than the administration of one of the several broad- by each of the single aetiological agents. This would be a spectrum parasiticides available on the market, even in the basic step to cope with current weaknesses in prevention absence of evident parasitosis or without a copromicro- approaches and to establish where to intervene with fo- scopic examination. Such a fallacy comes from the miscon- cused plans. In fact, updated information on prevalence ceptions that a deep knowledge of epidemiology and of parasites of dogs and cats and the risk factors asso- biology of certain parasites is superfluous and that control ciated with infection, as well as reinforcing veterinary of major helminths can be achieved just with a periodic and public health concerns, is of crucial relevance medication. Nonetheless, roundworms and hookworms re- because common awareness is non-existent or often main today the most diffused nematodes affecting pets based on outdated information. around the world and they still cause zoonotic infections in The cornerstone to control intestinal parasitoses of humans.Thereis,therefore,theevidence,thatscientists, pets is a combination of strategic worming methods pet owners and veterinarians should re-consider their ap- (especially puppies, kittens and dams), wearing footwear proach on parasitology and foster their interest not only in when needed, supervising playing children and their emergent parasites like cardio-pulmonary nematodes or interactions with pets, breaking faecal-oral routes by water-borne protozoa, but also in “old-fashioned” intestinal washing hands and removal and disposal of faeces from worms. Traversa Parasites & Vectors 2012, 5:91 Page 15 of 19 http://www.parasitesandvectors.com/content/5/1/91

Given that parasitic zoonoses are too often neglected 8. Antolová D, Reiterová K, Miterpáková M, Stanko M, Dubinský P: Circulation or underappreciated, and may be mismanaged or of Toxocara spp. in suburban and rural ecosystems in the Slovak Republic. Vet Parasitol 2004, 126:317–324. underdiagnosed by both veterinarians and physicians 9. Traversa D: Are we paying too much attention to cardio-pulmonary [213], a strong education outreach by veterinary and nematodes and neglecting old-fashioned worms like Trichuris vulpis? medical practitioners should be accomplished [214,220]. Parasit Vectors 2011, 4:32. 10. Lloyd S, Amersinghe PH, Soulsby EJL: Periparturient immunosuppression Veterinarians must keep their guard up against zoonotic in the bitch and its influence on infection with Toxocara canis. J Small parasitoses of pets and constantly provide advice and Anim Pract 1983, 24:237–247. improve knowledge of their clients, with a special focus 11. 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Lee CY, Schantz PM, Kazacos KR, Montgomery SP, Bowman DD: global worming, given that faster egg embryonation Epidemiologic and zoonotic aspects of ascarid infections in dogs and and increased over-wintering of infectious elements in cats. Trends Parasitol 2010, 26:155–161. the environment will likely increase the spread of 19. Parsons JC: Ascarid infections of cats and dogs. Vet Clin North Am Small Anim Pract 1987, 17:1307–1339. helminths affecting companion animals and humans in 20. Taylor MA, Coop RL, Wall RL: . 3rth edition.: Blackwell several areas of the World, as recently hypothesized Publishing; 2007. for sub-Arctic and Arctic regions [221]. 21. Sprent JF: Observations on the development of Toxocara canis (Werner, 1782) in the dog. Parasitology 1958, 48:184–209. 22. Prociv P: Zoonotic hookworm infections (Ancylostomosis).InIn Zoonoses. Competing interests 1st edition. Edited by Palmer SR, Soulsby EJL, Simpson DIH.: Oxford Medical Scientific aspects of the article have not been influenced by any third party. Publications; 1998. 23. Manning L, Chambers S, Paltridge G, Maurice P: Cutaneous larva migrans Acknowledgements (hookworm) acquired in Christchurch. New Zealand. N Z Med J 2006, – The author thanks Angela Di Cesare for the elaboration of bibliographic data, 119:1910 1913. Riccardo Lia for Figures 1 and 3D, Asaf Kohane for Figure 2 and Antonio 24. Palmer CS, Traub RJ, Robertson ID, Hobbs RP, Elliot A, While L, Rees R, Frangipane di Regalbono for Figure 3C. Thompson RC: The veterinary and public health significance of The author expresses his gratitude and devotion to his loves in Figure 5: hookworm in dogs and cats in Australia and the status of A. ceylanicum. – Alessandra, Maria, Pata, Inca, Ruffi and Trizma. Vet Parasitol 2007, 145:304 313. 25. 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